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Year: 2011
Deep brain stimulation in parkinsonian patients — ethical evaluation of
cognitive, affective, and behavioral sequelae
Müller, S; Christen, M
Abstract: Deep brain stimulation (DBS) of the subthalamic nucleus (STN) is an important therapeutic
advancement for the treatment of Parkinson’s disease (PD). Its beneficial effects on motor functions are
well established, but its cognitive, affective, and behavioral sequelae come increasingly into the focus
of the medical and ethical discussion. In order to evaluate whether these side effects may counteract
the beneficial effects of STN DBS on the patient’s quality of life, we classify them along the dimensions
“measurement complexity” and “weighted life-impact.” Based on this analysis, we discuss their ethical
impact and propose guidelines for the clinical setting of STN DBS.
DOI: https://doi.org/10.1080/21507740.2010.533151
Posted at the Zurich Open Repository and Archive, University of Zurich
ZORA URL: https://doi.org/10.5167/uzh-55241
Accepted Version
Originally published at:
Müller, S; Christen, M (2011). Deep brain stimulation in parkinsonian patients — ethical evaluation of
cognitive, affective, and behavioral sequelae. AJOB Neuroscience, 2(1):3-13.
DOI: https://doi.org/10.1080/21507740.2010.533151
American Journal of Bioethics - Neuroscience
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Journal:
Manuscript ID:
Manuscript Type:
AJOB Neuroscience Journal
UABN-2011-0047.R1
Target Article
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Keywords:
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Dealing with Side Effects of Deep Brain Stimulation: Lessons
Learned from Stimulating the STN
Deep Brain Stimulation, psychiatry, Harm, Neuroethics, Neurosurgery
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Dealing with Side Effects of Deep Brain Stimulation:
Lessons Learned from Stimulating the STN
Abstract
Deep brain stimulation (DBS) is increasingly investigated as a therapy for psychiatric
disorders. In the ethical evaluation of this novel approach, incidence and impact of side
effects (SE) play a key role. In our contribution, we analyze the discussion on SE of DBS of
the subthalamic nucleus (STN) – a standard therapy for movement disorders like Parkinson’s
disease (PD) – based on 66 case reports, 69 review papers, and 347 outcome studies from
1993 to 2009. We show how the DBS community increasingly acknowledged the complexity
of STN-DBS side effects. Then we discuss the issue of study quality and the methods used to
assess SE. We note that some side effects are subject of conflicting evaluations by the
different stakeholders involved. This complicates the ethical controversy inherent in any
novel treatments for diseases that involve psychiatric aspects. We delineate how the lessons
from STN-DBS could guide future DBS applications in the field of psychiatry.
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Key words: Deep brain stimulation, psychiatry, Parkinson’s disease, subthalamic nucleus,
side effects, neuroethics.
Introduction
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Since the advent of medicine, the maxim “do not harm your patient” forms the core of the
ethos for physicians. This is reflected in the principle of nonmaleficience as one of the four
principles of biomedical ethics (Beauchamp & Childress 2009). Nevertheless, it is broadly
acknowledged that harmful side effects (SE) of therapies have to be weighed up against their
beneficial effects. The deliberation of harms and benefits becomes more difficult if side
effects of novel therapeutic approaches have to be considered, of which nature, extent, and
incidence are not yet known.
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Deep brain stimulation (DBS) is an example for a novel therapeutic approach. Its roots go
back to the early 1950s (Hariz et al. 2010), and it emerged in its current form in the 1980s as
an alternative for ablative surgery in movement disorders and an experimental therapy in
chronic pain (Siegfried & Blons 1997). DBS became an established therapy for Parkinson’s
disease (PD) and other movement disorders in the last decade (Benabid et al. 2009). Side
effects have been discussed since the advent of DBS, but the sensibility for them and the
appreciation of their complexity is increasing. This also reflects the maturation of the therapy.
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American Journal of Bioethics - Neuroscience
The term ‘side effect’ does not provide per se an ethical orientation how to deal with a
specific therapy. Therefore terms like ‘adverse events’ or ‘sequelae’ (adverse events that
count as long-term negative consequences) should be avoided as long as the negative
evaluation of the side effect is not clear. For evaluating particular side effects, they can be
classified along the two dimensions predictability and evaluation (Table 1).
INSERT TABLE 1
Table 1:
Ethical requirements depending on the predictability and the evaluation of the side effects of a
therapy.
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American Journal of Bioethics - Neuroscience
As Table 1 shows, only one type of side effects (predictable and clearly outweighing the
benefits) bears the clear “ethical message” that the therapy should not be applied or that
research on this therapy should be stopped. Thus, the determination of what counts as an
adverse event involves both a measurement problem and an evaluation problem which can be
entangled in the process of developing the therapy (Müller & Christen 2011). DBS for PD
patients is a paradigmatic example for outlining that problem, since first the predictability of
side effects for individual patients is difficult, second the evaluation of some side effects
differs significantly between patients, their relatives and physicians (Müller & Christen 2011),
and third both the disease (Kulisevsky et al. 2008) and alternative therapeutic approaches
(medication or surgery, see Voon et al. 2006 and Olanow 2002) may involve similar effects as
DBS.
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The following investigation is based on a comprehensive literature analysis of the research
literature on DBS in the nucleus subthalamicus (STN), the preferred target for DBS in PD.
This analysis covers 66 case reports, 69 review papers, and 347 outcome studies from 1993 to
2009 that emerged from an extensive search in the following databases: CPCI-S, Embase,
Francis, Medline, PsychINFO and SCI-expanded (the reference lists are available as
supporting online material).
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As the STN is part of various thalamo-cortical circuits (Marani et al 2008), the relatively high
incidence of cognitive and affective side effects after STN DBS compared to other DBS
targets is not surprising (Hariz et al. 2008). The way the DBS community dealt with this issue
is thus a paradigmatic case for analyzing SE measurement and evaluation in the course of the
establishment of novel therapies. Understanding this process may support the ethical analysis
of the current application of DBS to a variety of psychiatric disorders (for an overview about
psychiatric DBS see Krack et al. 2010).
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The complexity of adverse events
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Since the early 1990s, the STN was investigated as a potential DBS target both in animal and
clinical studies. In 1993, the first case was published in a French journal (Pollak et al. 1993).
Several case reports and outcome studies followed, and since the late 1990s the number of
publications on STN-DBS has increased steadily (Müller & Christen 2011). The number of
STN-DBS related issues discussed in the literature has grown rapidly, whereas a bibliometric
investigation demonstrated that case reports spearhead the transdisciplinary communication
about DBS (Christen & Müller 2011).
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To handle the complexity of issues that are discussed in our literature body of 482 STN-DBS
publications, we have sorted them into 18 issue classes (Table 2). For each class, we have
evaluated all tests used in the outcome literature to measure the respective phenomena and the
wording used to describe the corresponding SE. Note that not each issue class is directly
related to SE. This is true especially for studies on the neuronal basis of DBS effects (usually
investigated by PET) or about the cost-effectiveness of DBS. Furthermore, the boundaries
between some issue classes are less clear and required predefinitions. For example, we have
classified studies about language fluency as ‘cognitive’ (in accordance with the current
neuropsychological understanding).
Each publication (case report, review, outcome study) was attributed to one or several issue
classes with regard to the topics discussed and the methods used. Thereby we did not take into
account possible causal relations between certain issues. For example, many issues have an
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impact on the quality of life (Q). Nevertheless, a study whose, e.g., primary focus was
insomnia was only classified as ‘I’, not as ‘Q’. For analyzing the time course of the
publication praxis, it was necessary to build bigger groups. Therefore we have grouped the 18
issue classes into four groups as follows:
1. Group: Understanding therapeutic effects: F, M, V
2. Group: Medical and technical intervention issues: O, P, T
3. Group: Main affective, behavioral and cognitive side effects of DBS: B, C, D, L, Q
4. Group: Other issues: A, E, I, K, N, S, W
INSERT TABLE 2
Table 2:
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Issue classes of therapeutic effects and side effects present in the STN-DBS literature. Only
selected examples of side effects using the wording found in the publications are displayed.
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The histogram in Fig. 1 shows the time-course of the different groups of issues in the DBS
literature. The absolute numbers of publications per year belonging to one of the four issue
groups are displayed for the years 1993 to 2009. The analysis reveals that – after the first,
pioneering years with very few studies – issues on main affective, behavioral and cognitive
side effects quickly appeared in the literature and became the dominant group since 2003.
This finding is corroborated by an analysis of DBS posters presented at conferences (Christen
& Müller 2011). Although one has to take into account that this analysis is not sensible for the
valuation of these effects (i.e. whether they are considered to be unproblematic or not), this
finding somehow contrasts with several statements in the literature, that the DBS community
would often ignore the neurobehavioral consequences of the therapy (e.g., Burn & Tröster
2004).
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INSERT FIGURE 1
Figure 1:
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The histogram displays the total number of issues (compare with Table 2) addressed in the
publications about STN-DBS (case reports, reviews, and outcome studies) pooled in four
groups (Group 1: F, M, V / Group 2: O, P, T / Group 3: B, C, D, L, Q / Group 4: A, E, I, K, N,
S, W; see text).
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Quality of STN-DBS studies
The sensibility for novel side effects in the process of maturation of a novel therapy is a
critical issue – and we may say that the DBS community has passed this test successfully.
Another issue is the quality of the studies. Although it is well-known that novel therapies start
with isolated case studies that usually lack quality criteria like randomization or blinding, at
some point the urge for better studies is raised. DBS did not deviate from this development
path, and various authors have discussed the issue of study quality (e.g. Woods et al. 2006)
and proposed standards for improving study quality (e.g. Morrison et al. 2000). We
investigated the study quality for all outcome studies that involved at least one issue of group
3 (i.e.: B, C, D, L, or Q). For that, we expanded the criteria for level of evidence assignment
proposed by Martinez-Martin & Deuschl (2007) using a rating system that involves several
aspects being considered as relevant for study quality (e.g. regarding follow-up time) by the
DBS community.i
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American Journal of Bioethics - Neuroscience
As Fig. 2.a demonstrates, the quality range of the studies is broad. Somewhat surprising is the
fact that the mean quality of the outcome studies did not increase significantly since 2000
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American Journal of Bioethics - Neuroscience
(Fig. 2.b; earlier studies where not taken into account due to their low numbers). Although the
absolute number of high quality studies of group 3 has increased, they are shrouded by the
also increasing number of outcome studies of poor quality.
This absent increase of the average study quality is not per se problematic, as long as the
community is able to differ between good and poor studies. To investigate whether this is the
case, we calculated a citation coefficient based on DBS review papers about the outcome
studies of group 3.ii Then we performed a correlation analysis of the relationship of this
citation coefficient and the quality rating for each study. The result is a (weak) positive
correlation of the citation coefficient with the quality rating (Pearson's correlation coefficient:
0.29). That means that high quality papers tend to be cited more often in the reviews. This can
be interpreted as a hint for a higher appreciation of high quality studies of group 3 by the DBS
community.
Figure 2:
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INSERT FIGURE 2
(a) Quality rating distribution of the outcome studies of group 3, (b) time-course of the mean
quality rating of outcome studies (group 3), (c) correlation between the citation coefficient of
studies (which reflects the appreciation of papers by the authors of reviews) with the quality
rating of the studies. The chart also includes the linear approximation of the correlation.
Measuring Adverse Events
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After investigating the attention for side effects of group 3 and the quality of the studies
investigating them, we investigated a third issue: To what extent do the studies capture
“relevant” side effects, i.e. those reflecting serious ethical issues (see Table 1). This point
requires a closer look to the methods and tests used in the outcome studies. We listed all tests
used in the 347 outcome studies and attributed them to one of the 18 issue groups. Far most of
the tests were assigned to one of the five issue classes B, C, D, L, and Q (group 3), whereas
the internal distribution is very uneven. Fig. 3.a demonstrates that more than half of all
methods applied are tests regarding cognitive issues. Also the number of uses of the tests
themselves is remarkably uneven. Only very few tests are used regularly. Furthermore, the
probability that a test is used in a study for neuropsychological outcome assessment does not
correspond completely to the four standards proposed in the literature (Defer et al. 1999,
Saint-Cyr et al. 2000, Morrison et al. 2000, Pillon 2002). For example, the Hopkins Verbal
Learning Test and the Odd Man Out Test, both recommended in all four standards, are
comparably rarely used. This may indicate a learning effect by the community, as better tests
than the ones initially recommended are available that measure similar constructs.
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For the ethical evaluation it is of particular interest which perspectives are represented in the
tests, as conflicting evaluations of side effects often result from different perspectives of
stakeholders. For analyzing this point, we have classified all tests as follows:
I)
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III)
Test scores that result from the evaluation of the patient’s performance by a trained
evaluator
Test scores that result from a self-assessment of the patient
Test scores that result from an interrogation etc. from closely related persons of the
patient (family members, caregivers)
In order to avoid biases due to low quality studies, we have only investigated those studies
that achieved a quality rating of at least 5 (see footnote 1, 182 studies). We have counted the
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number of different tests, the number of test executions (i.e. in how many studies the test was
used) and the number of patients that have been tested by these methods. The cumulative
numbers for the three classes I, II and III are displayed in Fig. 3.b.
INSERT FIGURE 3
Figure 3:
a: Number of tests per issue class (B: behavioral, C: cognitive, D: depression and other mood
issues, L: language, Q: quality of life). b: Number of different tests (first bar in each group), of
accumulated test executions (middle bar) and total number of patients tested (left bar, right
scale) with methods of either class I (test scores generated by evaluator), II (self-assessment of
patient) or III (test scores emerge from persons affiliated to the patient).
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We see a clear dominance of category I tests, whereas the usage of category III tests is
basically nonexistent. Thus, the perspective on side effects is very biased in the DBS
literature. This finding might explain the “satisfaction gap” between the physician’s and the
patient’s expectation that is discussed in the literature (Agid et al 2006).
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The Ethics of Adverse Events: Conclusions and Recommendations for Psychiatric DBS
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What is the impact of this in-depth analysis of the literature about side effects of STN-DBS
for the ethical debate about the application of DBS in psychiatry? Compared to many somatic
diseases, harm-benefit-assessments for psychiatric therapies are complicated by at least three
problems: First, for most psychiatric disorders no clear correlation with a specific
neurological dysfunction is proven. Second, many interventions affect various neuronal
mechanisms, e.g., SSRI have effects not only on the serotonin metabolism, but also on the
neurogenesis in the hippocampus (Santarelli et al. 2003). Third, the evaluation of both the
disease and the beneficial and negative therapy effects depend much stronger on subjective
evaluations than this is valid for the somatic medicine. For example, neither patients nor their
relatives nor their physicians would doubt that toothache is painful, whereas hypomania is
evaluated differently by different stakeholders (see e.g. the examples in Krug et al. 2010).
‘Clear-cut’ cases (predictable side effects that clearly outbalance therapeutic effects) are
probably rather rare in psychiatric diseases.
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This is important, since the introduction of DBS to psychiatry is driven also by the
expectation that it will improve the understanding of the causes of these diseases and that it
will be a causal therapy. Already the usage of DBS for the treatment of movement disorders
was accompanied by the narrative that DBS is more precise than its alternatives, completely
reversible, and individually scalable. Although this is to a large extent true, the problems of
measuring and evaluating side effects do not vanish. In the contrary, our analysis revealed that
the availability of a more precise tool triggered research on the mechanisms behind the effects
of DBS on cognitive functions, mood, and behavior and thus tends to increase the spectrum of
potential SE to look at. If DBS will play an important role in psychiatry, we cannot expect
that the SE spectrum will become smaller compared to that implicated by the alternatives.
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However, we have found a well-developed sensibility for side effects in the DBS community.
Nevertheless, the side effects are not yet measured and evaluated sufficiently. Our analysis
reveals that the majority of methods used investigate subtle cognitive changes which may be
statistically significant but whose relevance for the patients is unclear. Only a minority of
investigations focus on the self-assessment of the patients, and even less on the assessments of
their caregivers. This methodological bias implies blindness for certain side effects. We
expect that this problem will be aggravated if DBS is used to treat psychiatric disorders as
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American Journal of Bioethics - Neuroscience
depression or addiction, since interpersonal relationships play a crucial role in overcoming
these disorders.
Finally, the quality of studies that promote the extended use of DBS gives cause for concern,
although we note that our rating system does not take into account that the requirements for
quality may differ between studies if they addressed different types of outcomes, such that not
all quality items are required for a specific study. After all, progress is recognizable and the
community is somewhat able to discriminate between good and bad studies, yet it has not
managed to cut down the continuous generation of low quality contributions.
In summary, the ethical evaluation of side effects of STN-DBS must not abstract from the
measurement and evaluation problems that constitute the definition of what counts as a ‘side
effect’. The role of ethicists is not only to safeguard against the “bad effects” of therapies.
They should also point at blind spots in clinical studies and widen the perspective on all sorts
of effects of new therapies.
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This research has been supported by the Swiss Academy of Medical Sciences (Käthe-ZinggSchwichtenberg-Fonds) and by the Federal Ministry of Education and Research, Germany
(project no. 01 GP 0804).
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Brain Stimulation in Parkinson's Disease. The Clinical Neuropsychologist, 20(1): 27-38.
i
Each study was assigned with points as follows: Study was prospective: +1; study was case-controlled with at
least 20 participants in each branch: +2 (+1 if less than 20 participants in either branch); study was randomized:
+1; test evaluation was blinded: +1; study involved more than one center: +1; the pre-surgery and post-surgery
assessment of the neuropsychiatric tests were made in the “best” (pre: med-on/ post: med-on, stim-on) condition
of the patient: +2 (+1 if the assessments were made pre and post); the study involved at least 20 patients: +1; the
study had a follow-up time of at least 12 month: +1; the study involved tests of at least three issue classes: +1.
ii
The citation coefficient was construed as follows: We counted the appearance of outcome studies in the
analytic part of reviews that either performed a meta-analysis following established standards (e.g. Cochrane) or
were at least systematically evaluated (i.e. we excluded merely narrative reviews; thus we considered 23
reviews). The citation of outcome papers is weighted with the probability of being able to be cited due to the
year of publication to take into account, that a paper e.g. published in 2006 cannot be cited in a review published
in 2004. Thus each outcome paper received a citation coefficient value between 0 and 1. For the correlation
analysis, only outcomes with nonzero citation coefficient have been analyzed.
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The histogram displays the total number of issues (compare with Table 2) addressed in the
publications about STN-DBS (case reports, reviews, and outcome studies) pooled in four groups
(Group 1: F, M, V / Group 2: O, P, T / Group 3: B, C, D, L, Q / Group 4: A, E, I, K, N, S, W; see
text).
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(a) Quality rating distribution of the outcome studies of group 3, (b) time-course of the mean
quality rating of outcome studies (group 3), (c) correlation between the citation coefficient of
studies (which reflects the appreciation of papers by the authors of reviews) with the quality rating
of the studies. The chart also includes the linear approximation of the correlation.
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a: Number of tests per issue class (B: behavioral, C: cognitive, D: depression and other mood
issues, L: language, Q: quality of life). b: Number of different tests (first bar in each group), of
accumulated test executions (middle bar) and total number of patients tested (left bar, right scale)
with methods of either class I (test scores generated by evaluator), II (self-assessment of patient)
or III (test scores emerge from persons affiliated to the patient).
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American Journal of Bioethics - Neuroscience
Christen et al.: Dealing with Side Effects of Deep Brain Stimulation
Evaluation
Table 1
The SE of the therapy
clearly outweighs its
therapeutic effects.
There are conflicting
evaluations of the SE
by different
stakeholders.
The therapeutic
effects clearly
outbalance the SE.
Predictability of side effects (SE) of a therapy
predictable
not predictable
Do not begin / stop the therapy.
Ensure sensibility for novel SE.
Define the authority to decide about
the usage of the therapy.
Ensure involvement of different
stakeholder’s perspectives during the
development of the therapy.
Define a procedure to take individual
variability of the impact of the SE
into account.
Define a procedure to decide whether
a novel SE is classified as
unproblematic or not.
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Christen et al.: Dealing with Side Effects of Deep Brain Stimulation
Table 2
Group 1
Abbr.
F
M
V
P
T
B
L
Q
Examples of side effects
-
Apraxia, axial symptoms, dyskinesia, dystonia,
gait disorders, motor fluctuations
Dopamine dysregulation syndrome, changes in
LEDD
Hemorrhage, hematoma, ischemia, surgical
complications, infections
Battery problems, electrode break, local infections,
lead fracture, pulse generator malfunction
Compulsive shopping, hypersexuality, hypomania,
pathological gambling, suicide (attempts)
Cognitive decline, confusion, dementia, memory
decline, verbal fluency
Ahedonia, apathy, depression, mood changes,
sadness
Aphasia, dysarthria, hypophonia, speech
impairment, voice freezing
Disability in daily living, decreased life
satisfaction, partnership problems
Drooling, dysphagia, hyperhidrosis
E
Effects regarding the autonomous nervous
system, autonomous functioning
Emotion recognition changes
I
Insomnia, i.e. effects related to sleep
K
-
N
Cost issues (German: Kosten), i.e. cost-benefitstudies, cost-effectiveness of DBS etc.
Other neurological effects
S
Effects regarding sensory systems
Blurred vision, parasthesia, visual hallucinations
W
Weight and energy intake changes
Abnormal weight gain, binge eating, obesity
Difficulties of emotion discrimination, difficulties
of face perception, hyperemotivity
Drowsiness, fatigue, insomnia, sleep disorders
iew
Group 4
Depression, anxiety, apathy and other mood
effects
Language, i.e. effects regarding the general
speech ability and motor aspects of speech
Quality of life and social aspects
ev
A
Behavioral effects, i.e. effects that concern
abnormal behavior
Effects on cognition (reasoning, memory etc.)
rR
Group 3
D
Patient issues, i.e. issues related to patient
selection, patient management, rehabilitation
Effects related to the technology (device)
ee
C
Issues related to Levodopa and other
medication
Operation/surgery related issues
rP
Group 2
O
Issue class
Functional studies, i.e. studies that involve PET
or other methods for investigating the causal
effect of DBS
Motor effects
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Epilepsy, postural imbalance, seizures
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Christen M, Müller S, Bittlinger M, Walter H, and Brugger P: Dealing with Side Effects
of Deep Brain Stimulation: Lessons Learned from Stimulating the STN
Supplementary Material
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List of Review Papers (69)
Alberts JL, Hass CJ, Vitek JL, Okun MS. 2008. Are two leads always better than one: An emerging case for
unilateral subthalamic deep brain stimulation in Parkinson's disease. Experimental Neurology 214: 1–5
Amick MM, Grace J. 2006. Deep Brain Stimulation Surgery for Parkinson’s Disease: The Role of
Neuropsychological Assessment. Medicine and Health / Rhode Island 89(4): 130–133
Anderson KE, Mullins J. 2003. Behavioral changes associated with deep brain stimulation surgery for
Parkinson's disease. Current Neurology and Neuroscience Reports 3(4): 306–313
Appleby BS, Duggan PS, Regenberg A, Rabins PV. 2007. Psychiatric and neuropsychiatric adverse events
associated with deep brain stimulation: A meta-analysis of ten years' experience. Movement Disorders
22(12): 1722–1728
Ashkan K, Wallace B, Bell BA, Benabid AL. 2004. Deep brain stimulation of the subthalamic nucleus in
Parkinson’s Disease 1993 – 2003: where are we 10 years on? British Journal of Neurosurgery 18(1): 19–
34
Benabid AL. 2003. Deep brain stimulation for Parkinson’s disease. Current Opinion in Neurobiology 13: 696–
706
Benabid AL, Benazzouz A, Hoffmann D, Limousin P, Krack P, Pollak P. 1998. Long-term electrical inhibition
of deep brain targets in movement disorders. Movement Disorders 13 Suppl 3: 119–125.
Benabid AL, Chabardes S, Mitrofanis J, Pollak P. 2009. Deep brain stimulation of the subthalamic nucleus for
the treatment of Parkinson's disease. Lancet Neurology 8(1): 67–81
Benabid AL, Chabardès S, Seigneuret E. 2005. Deep-brain stimulation in Parkinson's disease: long-term efficacy
and safety – What happened this year? Current Opinion in Neurology 18(6): 623–30
Berney A, Vingerhoets F. 2004. Stimulation cérébrale profonde dans la maladie de Parkinson: effets moteurs et
comportementaux. Schweizer Archiv für Neurologie und Psychiatrie 155(8): 399–406
Boisson D. 2008. Stimulation cérébrale profonde et maladie de Parkinson. Annales de réadaptation et de
médecine physique 51 (2008) 491–500
Boucai L, Cerquetti D, Merello M. 2004. Functional surgery for Parkinson's disease treatment: a structured
analysis of a decade of published literature. British Journal of Neurosurgery 18(3): 213–223
Burkhard PR, Villemure J-G, Vingerhoets FJG. 2005. Current treatment of Parkinson's disease: Problems and
controversies. Revue Medicale Suisse 1(18): 1214–1219
Burn DJ, Tröster AI. 2004. Neuropsychiatric complications of medical and surgical therapies for Parkinson's
disease. Journal of Geriatry, Psychiatry and Neurology 17: 172–180
Defebvre l, Krystkowiak P, Blond S, Destée A. 2000. Stimulation électrique chronique du pallidum interne et du
noyau subthalamique dans la maladie de Parkinson. Presse Medicale 29: 1525–1531
Defer GL, Widner H, Marié RM, Rémy P, Levivier M. 1999. Core assessment program for surgical
interventional therapies in Parkinson's disease (CAPSIT–PD). Movement Disorders 14(4): 572–84
Deuschl G, Herzog J, Kleiner-Fisman G, Kubu C, Lozano AM, Lyons KE, Rodriguez-Oroz MC, Tamma F,
Troster AI, Vitek JL, Volkmann J, Voon V. 2006. Deep Brain Stimulation: Postoperative Issues.
Movement Disorders 21 (Suppl. 14): S219–S237
Deuschl G, Wenzelburger R, Kopper F, Volkmann J . 2003. Deep brain stimulation of the subthalamic nucleus
for Parkinson's disease: a therapy approaching evidence-based standards. Journal of Neurology 250(1):
I/43–I/46
Diamond A, Jankovic J. 2005. The effect of deep brain stimulation on quality of life in movement disorders.
Journal of Neurology, Neurosurgery & Psychiatry 76(9): 1188–1193
Dowsey-Limousin P, Pollak P. 2001. Deep brain stimulation in the treatment of Parkinson's disease: a review
and update. Clinical Neuroscience Research 1(6): 521–526
Drapier S, Damier P. 2003. Continuous subthalamic neurostimulation in Parkinson's disease – Indications and
modalities. Presse Medicale 32(28): 1334–1339
Fields Julie A, Tröster Alexander I. 2000. Cognitive Outcomes after Deep Brain Stimulation for Parkinson’s
Disease: A Review of Initial Studies and Recommendations for Future Research. Brain and Cognition 42,
268–293 (2000)
Fogel W, Krause M, Tronnier VM. 2000. Ergebnisse der STN–Stimulation im Vergleich mit anderen
stereotaktischen Verfahren. Akt Neurol 27 Supplement 1: S9—S15
Goetz CG, Poewe W, Rascol O, Sampaio C. . 2005. Evidence–based medical review update: pharmacological
and surgical treatments of Parkinson's disease: 2001 to 2004. Movement Disorders 20(5): 523–39.
Goodman RR, Kim B, McClelland III S, Senatus PB, Winfield LM, Pullman SL, Yu Q, Ford B, McKhann II
GM. 2006. Operative techniques and morbidity with subthalamic nucleus deep brain stimulation in 100
consecutive patients with advanced Parkinson’s disease. Journal of Neurology Neurosurgery and
Psychiatry 77: 12–17
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American Journal of Bioethics - Neuroscience
Hallett M, Litvan I. 1999. Evaluation of surgery for Parkinson's disease: a report of the Therapeutics and
Technology Assessment Subcommittee of the American Academy of Neurology. The Task Force on
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Halpern CH, Rick JH, Danish SF, Grossman M, Baltuch GH . 2009. Cognition following bilateral deep brain
stimulation surgery of the subthalamic nucleus for Parkinson's disease. International Journal of Geriatric
Psychiatry 24: 443–451
Hamani C, Lozano AM. 2006. Hardware-related complications of deep brain stimulation: a review of the
published literature. Stereotactic and Functional Neurosurgery 84: 248–51
Hamani C, Richter E, Schwalb JM, Lozano AM. 2005. Bilateral subthalamic nucleus stimulation for Parkinson's
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Hariz MI. 2000. Pros and Cons of Various stereotactic procedures for Parkinson's Disease. Pan Arab
Neurosurgery 4(2)
Hariz MI. 2002. Complications of deep brain stimulation. Movement disorders 17(S3): S162–166
Herzog J, Deuschl G, Volkmann J. 2003. Deep brain stimulation in the treatment of idiopathic Parkinson's
disease. Nervenheilkunde: Zeitschrift für interdisziplinaere Fortbildung 22(10): 498–503
Herzog J, Deuschl G, Volkmann J. 2008. Tiefe Hirnstimulation bei der Parkinsonschen Krankheit.
Nervenheilkunde 27: 403–412
Israel Z, Hassin-Baer S. 2005. Subthalamic Stimulation for Parkinson’s Disease. IMAJ 7: 458–463
Karner E, Wolf E, Poewe W, Benke T. 2004. Neuropsychologische Befunde bei Stimulation der Basalganglien –
ein Review. Zeitschrift für Neuropsychologie, 15 (4), 2004, 287–301
Kirsch-Darrow L, Mikos A, Bowers D. 2008. Does deep brain stimulation induce apathy in parkinson’s disease?
Frontiers in Bioscience May 1: 5316–5322
Kleiner-Fisman G, Herzog J, Fisman DN, Tamma F, Lyons KE, Pahwa R, Lang AE, Deuschl G. 2006.
Subthalamic Nucleus Deep Brain Stimulation: Summary and Meta-Analysis of Outcomes. Movement
Disorders 21(14): S290–S304
Koller WC, Pahwa R, Lyons KE, Albanese A. 1999. Surgical treatment of Parkinson's disease. Journal of the
Neurological Sciences 167(1): 1–10
Krack P, Fraix V, Mendes A, Benabid A–L, Pollak P. 2002. Postoperative Management of Subthalamic Nucleus
Stimulation for Parkinson’s Disease. Movement Disorders 17 (Suppl. 3): S188–S197
Krack P, Hamel W, Mehdorn HM, Deuschl G . 1999. Surgical treatment of Parkinson's disease. Current Opinion
in Neurology 12(4): 417–25
Lefaucheur J-P, Gurruchaga J-M, Pollin B, von Raison F, Mohsen N, Shin M, Ménard–Lefaucheur I, Oshino S,
Kishima H, Fénelon G, Rémy P, Cesaro P, Gabriel I, Brugières P, Keravel Y, Nguyen J-P. 2008. Outcome
of Bilateral Subthalamic Nucleus Stimulation in the Treatment of Parkinson’s Disease: Correlation with
Intra-Operative Multi-Unit Recordings but Not with the Type of Anaesthesia. European Neurology 60:
186–199
Limousin P, Martinez–Torres I. 2008. Deep brain Stimulation for Parkinson's Disease. Neurotherapeutics 5:
309–319
Limousin-Dowsey P, Pollak P, Van Blercom N, Krack P, Benazzouz A, Benabid AL. 1999. Thalamic,
subthalamic nucleus and internal pallidum stimulation in Parkinson’s disease. Journal of Neurology 246
(Suppl. 2): II/42–II/45
Martinez-Martin P, Deuschl G. 2007. Effect of medical and surgical interventions on health-related quality of
life in Parkinson's disease. Movement Disorders 22(6): 757–65.
Meagher LJ, Ilchef R, Silberstein P, Cook RJ, Wasson D, Malhi GS. 2008. Psychiatric morbidity in patients with
Parkinson’s disease following bilateral subthalamic deep brain stimulation: literature review. Acta
Neuropsychiatrica 20: 182–192
Morrison CE, Borod JC, Brin MF, Raskin SA, Germano IM, Weisz DJ, Olanow CW. 2000. A program for
neuropsychological investigation of deep brain stimulation (PNIDBS) in movement disorder patients:
Development, Feasibility, and preliminary data. Neuropsychiatry, Neuropsychology and Behavioral
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Okun MS, Rodriguez RL, Mikos A, Miller K, Kellison I, Kirsch–Darrow L, Wint DP, Springer U, Fernandez
HH, Foote KD, Crucian G, Bowers D. 2007. Deep brain stimulation and the role of the neuropsychologist.
Clinical Neuropsychology 21(1):162–189
Olanow CW, Brin MF, Obeso JA. 2000. The role of deep brain stimulation as a surgical treatment for
Parkinson's disease. Neurology 55(12) Supplement 6: S60–S66
Panikar D, Kishore A. 2003. Deep brain stimulation for Parkinson's disease. Neurology India 51(2): 167–75
Parsons TD, Rogers SA, Braaten AJ, Woods SP, Tröster AI. 2006. Cognitive sequelae of subthalamic nucleus
deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurology 5: 578–588
Piasecki SD, Jefferson JW. 2004. Psychiatric Complications of Deep Brain Stimulation for Parkinson’s Disease.
Journal of Clinical Psychiatry 65: 845–849
Pillon B. 2002. Neuropsychological Assessment for Management of Patients with deep brain stimulation.
Movement Disorders 17(supplement 3): S116–S122
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Robert G, Drapier D, Verin M, Millet B, Azulay JP, Blin O. 2009. Cognitive impulsivity in Parkinson's disease
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Saint-Cyr JA, Trepanier LL. 2000. Neuropsychologic Assessment of Patients for Movement Disorder Surgery.
Movement Disorders 15(5): 771–783
Saleh C, Okun MS. 2008. A clinical review of deep brain stimulation and its effects on limbic basal ganglia
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Shih LC, Tarsy D. 2007. Deep Brain Stimulation for the Treatment of Atypical Parkinsonism. Movement
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Siegfried J, Blons S. 1997. The Neurosurgical treatment of Parkinson's disease and other movement disorders.
William & Wilkins Europe Ltd, London
Skidmore FM, Rodriguez RL, Fernandez HH, Goodman WK, Foote KD, Okun MS. 2006. Lessons Learned in
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Starr PA, Vitek JL, Bakay RA. . 1998. Ablative surgery and deep brain stimulation for Parkinson's disease.
Neurosurgery 43(5): 989–1013
Takeshita S, Kurisu K, Trop L, Arita K, Akimitsu T, Verhoeff NPLG. 2005. Effect of subthalamic stimulation
on mood state in Parkinson's disease: evaluation of previous facts and problems. Neurosurgical Review
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Temel Y, Kessels A, Tan S, Topdag A, Boon P, Visser-Vandewalle V. 2006. Behavioural changes after bilateral
subthalamic stimulation in advanced Parkinson disease: A systematic review. Parkinsonism and Related
Disorders 12: 265–272
Tröster AI. 2009. Cognitive and mood effects of subthalamic deep brain stimulation inParkinson's disease.
Minerva Psichiatrica 50(1): 79–92
Videnovic A, Metman LV. 2008. Deep Brain Stimulation for Parkinson’s Disease: Prevalence of Adverse Events
and Need for Standardized Reporting. Movement Disorders 23(3): 343–349
Voon V, Moro E, Saint-Cyr JA, Lozano AM, Lang AE. 2005. Psychiatric Symptoms following surgery for
Parkinson's disease with an emphasis on subthalamic stimulation. In: WJ Weiner, KE Anderson, AE Lang:
Behavioral neurology of movement disorders. Advances in Neurology 96 (2. edition). Lippincott Williams
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Voon V, Kubu C, Krack P, Houeto J-L, Troster AI. 2006. Deep Brain Stimulation: Neuropsychological and
Neuropsychiatric Issues. Movement Disorders 21 (Suppl. 14): S305–S326
Wolters EC. 2007. Deep brain stimulation and continuous dopaminergic stimulation in advanced Parkinson's
disease. Parkinsonism and Related Disorders 13: S18–S23
Woods SP, Fields JA, Tröster AI. 2002. Neuropsychological Sequelae of Subthalamic Nucleus Deep Brain
Stimulation in Parkinson’s Disease: A Critical Review. Neuropsychology Review 12(2): 111–126
Woods SP, Rippeth JD, Conover E, Carey CL, Parsons TD, Tröster AI. 2006. Statistical Power of Studies
Examining the Cognitive Effects of Subthalamic Nucleus Deep Brain Stimulation in Parkinson's Disease.
The Clinical Neuropsychologist, 20(1): 27–38
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Aybek S, Lazeyras F, Gronchi-Perrin A, Burkhard PR, Villemure JG, Vingerhoets FJ. 2009. Hippocampal
atrophy predicts conversion to dementia after STN–DBS in Parkinson's disease. Parkinsonism and Related
Disorders 15(7): 521–4
Accolla E, Caputo E, Cogiamanian F, Tamma F, Mrakic–Sposta S, Marceglia S, Egidi M, Rampini P, Locatelli
M, Priori A. 2007. Gender differences in patients with Parkinson's disease treated with subthalamic deep
brain stimulation. Movement Disorders 22(8): 1150–1156
Agostino R, Dinapoli L, Modugno N, Iezzi E, Gregori B, Esposito V, Romanelli P, Berardelli A. 2008.
Ipsilateral sequential arm movement after unilateral subthalamic deep brain stimulation in Patients with
Parkinson's disease. Movement Disorders 23(12): 1718–1724
Albanese A, Piacentini S, Romito LMA, Leone M, Franzini A, Broggi G, Bussone G, Burkhard PR, Ghika J,
Berney A, Villemure J–G, Vingerhoets FJG. 2005. Suicide after successful deep brain stimulation for
movement disorders. Neurology 65(3): 499
Alberts JL, Okun MS, Vitek JL. 2008. The persistent effect of unilateral pallidal and subthalamic deep brain
stimulation on force control in advanced Parkinson's patients. Parkinsonism and related disorders 14: 481–
488
URL: http://mc.manuscriptcentral.com/uabn Email: [email protected]
American Journal of Bioethics - Neuroscience
Alberts JL, Voelcker–Rehage C, Hallahan K, Vitek M, Bamzai R, Vitek JL. 2008. Bilateral subthalamic
stimulation impairs cognitive–motor performance in Parkinson's disease patients. Brain 131: 3348–3360
Alegret M, Junqué C, Valldeoriola F, Vendrell P, Pilleri M, Rumià J, Tolosa E. 2001. Effects of Bilateral
Subthalamic Stimulation on Cognitive Function in Parkinson Disease. Arch Neurol 58(8):1223–1227
Amirnovin R, Williams ZM, Cosgrove GR, Eskandar EN. 2006. Experience with microelectrode guided
subthalamic nucleus deep brain stimulation. Neurosurgery 58 (suppl): S96–102.
Anderson VC, Burchiel KJ, Hogarth P, Favre J, Hammerstad JP. 2005. Pallidal vs Subthalamic Nucleus Deep
Brain Stimulation in Parkinson Disease. Archives of Neurology 62(4): 554–560
Anheim M, Fraix V, Chabardès S, Krack P, Benabid AL, Pollak P. 2007. Lifetime of Itrel II pulse generators for
subthalamic nucleusstimulation in Parkinson’s disease. Mov Disord 22: 2436–39.
Anheim M, Batir A, Fraix V, Silem M, Chabardès S, Seigneuret E, Krack P, Benabid AL, Pollak P. 2008.
Improvement in Parkinson Disease by Subthalamic Nucleus Stimulation Based on Electrode Placement.
Effects of Reimplantation. Arch Neurol 65(5): 612–616
Arai N, Yokochi F, Ohnishi T, Momose T, Okiyama R, Taniguchi M, Takahashi H, Matsuda H, Ugawa Y. 2008.
Mechanisms of unilateral STN–DBS in patients with Parkinson's disease. A PET study. Journal of
Neurology 255: 1236–1243
Ardouin C, Pillon B, Peiffer E, Bejjani P, Limousin P, Damier P, Arnulf I, Benabid AL, Agid Y, Pollak P. 1999.
Bilateral subthalamic or pallidal stimulation for Parkinson's disease affects neither memory nor executive
functions: A consecutive series of 62 patients. Annals of Neurology 46(2): 217–223
Ardouin C, Voon V, Worbe Y, Abouazar N, Czernecki V, Hosseini H, Pelissolo A, Moro E, Lhommee E, Lang
AE, Agid Y, Benabid A–L, Pollak P, Mallet L, Krack P. 2006. Pathological Gambling in Parkinson’s
Disease Improves on Chronic Subthalamic Nucleus Stimulation. Movement Disorders 21(11): 1941–1946
Arnulf I, Bejjani BP, Garma L, Bonnet AM, Houeto JL, Damier P, Derenne JP, Agid Y. 2000. Improvement of
sleep architecture in PD with subthalamic nucleus stimulation. Neurology 55: 1732–35.
Aybek S, Gronchi–Perrin A, Berney A, Catalano Chiuvé S, Villemure J–G, Burkhard PR, Vingerhoets FJG.
2007. Long–term cognitive profile and incidence of dementia after STN–DBS in Parkinson's disease.
Movement Disorders 22(7): 974–981
Ballanger B, van Eimeren T, Moro E, Lozano AM, Hamani C, Boulinguez P, Pellecchia G, Houle S, Poon YY,
Lang AE, Strafella AP. 2009. Stimulation of the subthalamic nucleus and impulsivity: release your horses.
Ann Neurol. 66(6): 817–24
Bannier S, Montaurier C, Derost PP, Ulla M, Lemaire J–J, Boirie Y, Morio B, Durif F . 2009. Overweight after
deep brain stimulation of the subthalamic nucleus in Parkinson disease: long term follow–up. Journal of
Neurology Neurosurgery and Psychiatry 80(5): 484–488
Bannier S, Montaurier C, Derost PP, Ulla M, Lemaire J–J, Boirie Y, Morio B, Durif F. 2008. Overweight after
deep brain stimulatiuon of the subthalamic nucleus in Parkinson disease: long term follow up. J neurol
neurosurg psychiatry 80: 484–488
Barichella M, Marczewska AM, Mariani C, Landi A, Vairo A, Pezzoli G. 2003. Body weight gain rate in
patients with Parkinson's disease and deep brain stimulation. Movement Disorders 18(11): 1337–1340
Bastian AJ, Kelly VE, Revilla FJ, Perlmutter JS, Mink JW. . 2003. Different effects of unilateral versus bilateral
subthalamic nucleus stimulation on walking and reaching in Parkinson’s disease. . Mov Disord 18: 1000–
07.
Bejjani BP, Dormont D, Pidoux B, Yelnik J, Damier P, Arnulf I, Bonnet A–M, Marsault C, Agid Y, Philippon J,
Cornu P. 2000. Bilateral subthalamic stimulation for Parkinson's disease by using three–dimensional
stereotactic magnetic resoonance imaging and electrophysiological guidance. J Neurosurg 92: 615–625
Bejjani B–P, Gervais D, Arnulf I, Papadopoulos S, Demeret S, Bonnet A–M, Cornu P, Damier P, Agid Y. 2000.
Axial parkinsonian symptoms can be improved: the role of levodopa and bilateral subthalamic stimulation.
J Neurol Neurosurg Psychiatry 68: 595–600
Benabid A–L, Koudsié A, Benazzouz A, Fraix V, Ashraf A, Le Bas JF, Chabardes S, Pollak P. 2000.
Subthalamic stimulation for Parkinson's Disease. Archives of Medical Research 31: 282–289
Benabid AL, Krack P, Benazzouz A, Limousin P, Koudsie A, Pollak P. 2000. Deep brain stimulation of the
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Beric A, Kelly PJ, Rezai A, Sterio D, Mogilner A, Zonenshayn M, Kopell B. 2001. Complications of deep brain
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Berney A, Panisset M, Sadikot AF, Ptito A, Dagher A, Fraraccio M, Savard G, Pell M, Benkelfat C. 2007. Mood
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Berney A, Vingerhoets F, Perrin A, Guex P, Villemure J–G, Burkhard PR, Benkelfat C, Ghika J. 2002. Effect on
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Binder DK, Rau GM, Starr PA. 2005. Risk factors for hemorrhage during microelectrode–guided deep brain
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Biseul I, Sauleau P, Haegelen C, Trebon P, Drapier D, Raoul S, Drapier S, Lallement F, Rivier I, Lajat Y, Verin
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Blomstedt P, Hariz MI. 2006. Are Complications Less Common in Deep Brain Stimulation than in Ablative
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Blomstedt P, Hariz MI. 2005. Hardware–related complications of deep brain stimulation: a ten year experience. .
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Bordini BJ, Garg A, Gallagher CL, Bell B, Garell PC. 2007. Neuropsychological effects of bilateral deep brain
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Broggi G, Franzini A, Ferroli P, Servello D, D'Incerti L, Genitrini S, Soliveri P, Girotti F, Caraceni T. 2001.
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Brown RG, Dowsey PL, Brown P, Jahanshahi M, Pollak P, Benabid AL, Rodriguez–Oroz MC, Obeso J,
Rothwell JC. . 1999. Impact of deep brain stimulation on upper limb akinesia in Parkinson's disease. Ann
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Brusa L, Pierantozzi M, Peppe A, Altibrandi MG, Giacomini P, Mazzone P, Stanzione P. 2001. Deep brain
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Burchiel KJ, Anderson VC, Favre J, Hammerstad JP. 1999. Comparison of pallidal and subthalamic nucleus
deep brain stimulation for advanced Parkinson's disease: Results of a randomized, blinded pilot study.
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Burkhard PR, Vingerhoets FJG, Berney A, Bogousslavsky J, Villemure J–G, Ghika J. 2004. Suicide after
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Cantiniaux S, Vaugoyeau M, Robert D, Horrelou–Pitek C, Mancini J, Witjas T, Azulay JP. 2009. Comparative
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Capecci M, Ricciuti RA, Burini D, Bombace VG, Provinciali L, Iacoangeli M, Scerrati M, Ceravolo MG. 2005.
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